Skip to main content
SpringerLink
Log in

Interactions between biochar and mycorrhizal fungi in a water-stressed agricultural soil

  • Original Article
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Biochar may alleviate plant water stress in association with arbuscular mycorrhizal (AM) fungi but research has not been conclusive. Therefore, a glasshouse experiment was conducted to understand how interactions between AM fungi and plants respond to biochar application under water-stressed conditions. A twin chamber pot system was used to determine whether a woody biochar increased root colonisation by a natural AM fungal population in a pasture soil (‘field’ chamber) and whether this was associated with increased growth of extraradical AM fungal hyphae detected by plants growing in an adjacent (‘bait’) chamber containing irradiated soil. The two chambers were separated by a mesh that excluded roots. Subterranean clover was grown with and without water stress and harvested after 35, 49 and 63 days from each chamber. When biochar was applied to the field chamber under water-stressed conditions, shoot mass increased in parallel with mycorrhizal colonisation, extraradical hyphal length and shoot phosphorus concentration. AM fungal colonisation of roots in the bait chamber indicated an increase in extraradical mycorrhizal hyphae in the field chamber. Biochar had little effect on AM fungi or plant growth under well-watered conditions. The biochar-induced increase in mycorrhizal colonisation was associated with increased growth of extraradical AM fungal hyphae in the pasture soil under water-stressed conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abbott LK (1982) Comparative anatomy of vesicular-arbuscular mycorrhizas formed on subterranean clover. Aust J Bot 30:485–499

    Article  Google Scholar 

  • Abbott LK, Gazey C (1994) An ecological view of the formation of VA mycorrhizas. Plant Soil 159:69–78

    Google Scholar 

  • Abbott LK, Robson AD (1981) Infectivity and effectiveness of vesicular arbuscular mycorrhizal fungi: effect of inoculum type. Aust J Agric Res 32:631–639

    Article  Google Scholar 

  • Abbott LK, Robson AD (1984) The effect of root density, inoculum placement and infectivity of inoculum on the development of vesicular-arbuscular mycorrhizas. New Phytol 97:285–289

    Article  Google Scholar 

  • Abbott LK, Robson AD (1985) Formation of external hyphae in soil by four species of vesicular‐arbuscular mycorrhizal fungi. New Phytol 99:245–255

    Article  Google Scholar 

  • Abbott LK, Robson AD, Jasper DA, Gazey C (1992) What is the role of VA mycorrhizal hyphae in soil? In: Read DJ et al (eds) Mycorrhizas in ecosystems. CAB International, Wallingford, pp 37–41

    Google Scholar 

  • Abiven S, Hund A, Martinsen V, Cornelissen G (2015). Biochar amendment increases maize root surface areas and branching: a shovelomics study in Zambia. Plant and Soil 1–11

  • Al-Karaki G, McMichael B, Zak J (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 14:263–269

    Article  PubMed  Google Scholar 

  • Atkinson CJ, Fitzgerald JD, Hipps NA (2010) Potential mechanisms for achieving agricultural benefits from biochar application to temperate soils: a review. Plant Soil 337:1–18

    Article  CAS  Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381

    Article  Google Scholar 

  • Baronti S, Vaccari FP, Miglietta F, Calzolari C, Lugato E, Orlandini S, Pini R, Zulian L, Genesio L (2014) Impact of biochar application on plant water relations in Vitis vinifera (L.). Eur J Agron 53:38–44

    Article  CAS  Google Scholar 

  • Blackwell P, Riethmuller G, Collins M (2009) Biochar application to soil. In: Lehmann J, Joseph S (eds) Biochar for environmental management: science and technology. Earthscan, London, pp 207–226

    Google Scholar 

  • Borken W, Matzer E (2009) Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Glob Chang Biol 15:808–824

    Article  Google Scholar 

  • Bruun EW, Petersen CT, Hansen E, Holm JK, Hauggaard‐Nielsen H (2014) Biochar amendment to coarse sandy subsoil improves root growth and increases water retention. Soil Use Manag 30:109–118

    Article  Google Scholar 

  • Copley TR, Aliferis KA, Jabaji S (2015) Maple bark biochar affects Rhizoctonia solani metabolism and increases damping-off severity. Phytopathology 105:1334–1346

    Article  CAS  PubMed  Google Scholar 

  • Das O, Sarmah AK (2015) The love-hate relationship of pyrolysis biochar and water: a perspective. Sci Total Environ 512:682–685

    Article  PubMed  Google Scholar 

  • Degens BP, Sparling GP, Abbott LK (1996) Increasing the length of hyphae in a sandy soil increases the amount of water-stable aggregates. Appl Soil Ecol 3:149–159

    Article  Google Scholar 

  • Eason WR, Newman EI, Chuba PN (1991) Specificity of interplant cycling of phosphorus: the role of mycorrhizas. Plant Soil 137:267–274

    Article  CAS  Google Scholar 

  • Elzobair KA, Stromberger ME, Ippolito JA, Lentz RD (2016) Contrasting effects of biochar versus manure on soil microbial communities and enzyme activities in an Aridisol. Chemosphere 142:145–152

    Article  CAS  PubMed  Google Scholar 

  • Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530

    Article  PubMed  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Hall DJM, Jones HR, Crabtree WL, Daniels TL (2010) Claying and deep ripping can increase crop yields and profits on water repellent sands with marginal fertility in southern Western Australia. Soil Res 48:178–187

    Article  Google Scholar 

  • Hammer EC, Balogh-Brunstad Z, Jakobsen I, Olsson PA, Stipp SL, Rillig MC (2014) A mycorrhizal fungus grows on biochar and captures phosphorus from its surfaces. Soil Biol Biochem 77:252–260

    Article  CAS  Google Scholar 

  • Hammer EC, Forstreuter M, Rillig MC, Kohler J (2015) Biochar increases arbuscular mycorrhizal plant growth enhancement and ameliorates salinity stress. Appl Soil Ecol 96:114–121

    Article  Google Scholar 

  • Isbell R (2002) The Australian soil classification (Vol. 4). CSIRO Publishing

  • Jaafar NM (2014) Biochar as a habitat for arbuscular mycorrhizal fungi. In: Solaiman ZM, Abbott LK, Varma A (Eds) Mycorrhizal Fungi: Use in Sustainable Agriculture and Land Restoration. Soil Biol 41: 297–313

  • Jaafar NM, Clode PL, Abbott LK (2014) Microscopy observations of habitable space in biochar for colonization by fungal hyphae from soil. J Integr Agric 13:483–490

    Article  Google Scholar 

  • Jaafar NM, Clode PL, Abbott LK (2015) Soil microbial responses to biochars varying in particle size, surface and pore properties. Pedosphere 25:770–780

    Article  Google Scholar 

  • Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum. New Phytol 120:371–380

    Article  CAS  Google Scholar 

  • Jeong CY, Dodla SK, Wang JJ (2016) Fundamental and molecular composition characteristics of biochars produced from sugarcane and rice crop residues and by-products. Chemosphere 142:4–13

    Article  CAS  PubMed  Google Scholar 

  • Johnson CM, Ulrich A (1959) Analytical methods for use in plant analysis. Calif Agric Exp Sta Bull 767:25–78

    Google Scholar 

  • Jones DL, Rousk J, Edwards-Jones G, DeLuca TH, Murphy DV (2012) Biochar-mediated changes in soil quality and plant growth in a three year field trial. Soil Biol Biochem 45:113–124

    Article  CAS  Google Scholar 

  • Joseph SD, Camps-Arbestain M, Lin Y, Munroe P, Chia CH, Hook J, van Zwieten L, Kimber S, Cowie A, Singh BP, Lehmann J, Foidl N, Smernik RJ, Amonette JE (2010) An investigation into the reactions of biochar in soil. Soil Res 48:501–515

    Article  CAS  Google Scholar 

  • Kammann CI, Linsel S, Gößling JW, Koyro HW (2011) Influence of biochar on drought tolerance of Chenopodium quinoa Willd and on soil–plant relations. Plant Soil 345:195–210

    Article  CAS  Google Scholar 

  • Karhu K, Mattila T, Bergström I, Regina K (2011) Biochar addition to agricultural soil increased CH4 uptake and water holding capacity–results from a short-term pilot field study. Agric Ecosyst Environ 140:309–313

    Article  CAS  Google Scholar 

  • Khalvati MA, Hu Y, Mozafar A, Schmidhalter U (2005) Quantification of water uptake by arbuscular mycorrhizal hyphae and its significance for leaf growth, water relations, and gas exchange of barley subjected to drought stress. Plant Biol 7:706–713

    Article  CAS  PubMed  Google Scholar 

  • Kirono DGC, Kent DM, Hennessy KJ, Mpelasoka F (2011) Characteristics of Australian droughts under enhanced greenhouse conditions: results from 14 global climate models. J Arid Environ 75:566–575

    Article  Google Scholar 

  • LeCroy C, Masiello CA, Rudgers JA, Hockaday WC, Silberg JJ (2013) Nitrogen, biochar, and mycorrhizae: alteration of the symbiosis and oxidation of the char surface. Soil Biol Biochem 58:248–254

    Article  CAS  Google Scholar 

  • Lehmann J, Joseph S (2009) Biochar for environmental management: science and technology. (Eds J. Lehmann & S. Joseph) Earthscan, Dunstan house 14a St Cross Street London, EC1N 8XA

  • Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota—a review. Soil Biol Biochem 43:1812–1836

    Article  CAS  Google Scholar 

  • Liang C, Zhu X, Fu S, Méndez A, Gascó G, Paz-Ferreiro J (2014) Biochar alters the resistance and resilience to drought in a tropical soil. Environ Res Lett 9:064013

    Article  Google Scholar 

  • Major J, Lehmann J, Rondon M, Goodale C (2010) Fate of soil-applied black carbon: downward migration, leaching and soil respiration. Glob Chang Biol 16:1366–1379

    Article  Google Scholar 

  • McNamara NP, Black HIJ, Beresford NA, Parekh NR (2003) Effects of acute gamma irradiation on chemical, physical and biological properties of soils. Appl Soil Ecol 24:117–132

    Article  Google Scholar 

  • Mickan B (2014) Mechanisms for alleviating of water stress involving arbuscular mycorrhizal fungi. In: Solaiman ZM, Abbott LK, Varma A (Eds) Mycorrhizal Fungi: Use in Sustainable Agriculture and Land Restoration. Soil Biol 41:225–239

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Analyt Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Nzanza B, Marais D, Soundy P (2012) Effect of arbuscular mycorrhizal fungal inoculation and biochar amendment on growth and yield of tomato. Inter J Agri Biol 14:965–969

    CAS  Google Scholar 

  • Ogawa M, Okimori Y (2004) Pioneering works in biochar research, Japan. Aust J Soil Res 48:489–500

    Article  Google Scholar 

  • Ojeda G, Mattana S, Àvila A, Alcañiz JM, Volkmann M, Bachmann J (2015) Are soil-water functions affected by biochar application? Geoderma 249:1–11

    Article  Google Scholar 

  • Prendergast-Miller MT, Duvall M, Sohi SP (2011) Localisation of nitrate in the rhizosphere of biochar-amended soils. Soil Biol Biochem 43:2243–2246

    Article  CAS  Google Scholar 

  • Quilliam RS, Marsden KA, Gertler C, Rousk J, DeLuca TH, Jones DL (2012) Nutrient dynamics, microbial growth and weed emergence in biochar amended soil are influenced by time since application and reapplication rate. Agric Ecosyst Environ 158:192–199

    Article  CAS  Google Scholar 

  • Rillig MC (2004) Arbuscular mycorrhizae, glomalin and soil aggregation. Can J Soil Sci 84:355–363

    Article  Google Scholar 

  • Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317

    Article  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Azcon R, Gomez M (1995) Effects of arbuscular-mycorrhizal Glomus species on drought tolerance: physiological and nutritional plant responses. Appl Environ Microbiol 61:456–460

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Lozano JM, Porcel R, Bárzana G, Azcón R, Aroca R (2012) Contribution of arbuscular mycorrhizal symbiosis to plant drought tolerance: state of the art. In: Aroca P (ed) Plant Responses to Drought Stress. Springer, Berlin, pp 335–362

    Chapter  Google Scholar 

  • Ruth B, Khalvati M, Schmidhalter U (2011) Quantification of mycorrhizal water uptake via high-resolution on-line water sensors. Plant Soil 342:459–468

    Article  CAS  Google Scholar 

  • Shi P, Abbott LK, Banning NC, Zhao B (2012) Comparison of morphological and molecular genetic quantification of relative abundance of arbuscular mycorrhizal fungi within roots. Mycorrhiza 22:501–513

    Article  CAS  PubMed  Google Scholar 

  • Simard SW, Beiler KJ, Bingham MA, Deslippe JR, Philip LJ, Teste F (2012) Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol Rev 26:39–360

    Article  Google Scholar 

  • Solaiman ZM, Blackwell P, Abbott LK, Storer P (2010) Direct and residual effect of biochar application on mycorrhizal root colonization, growth and nutrition of wheat. Aust J Soil Res 48:546–554

    Article  CAS  Google Scholar 

  • Solaiman ZM, Murphy DV, Abbott LK (2012) Biochars influence seed germination and early growth of seedlings. Plant Soil 353:273–287

    Article  CAS  Google Scholar 

  • Stotzky G, Mortensen JL (1959) Effect of gamma radiation on growth and metabolism of microorganisms in an organic soil. Proc Soil Sci Soc Am 23:125–127

    Article  CAS  Google Scholar 

  • Taffouo VD, Ngwene B, Akoa A, Franken P (2013) Influence of phosphorus application and arbuscular mycorrhizal inoculation on growth, foliar nitrogen mobilization, and phosphorus partitioning in cowpea plants. Mycorrhiza 24:361–368

    Article  PubMed  Google Scholar 

  • Talmon Y, Sternberg M, Grynzweig J (2011) Impact of rainfall manipulations and biotic controls on soil respiration in Mediterranean and desert ecosystems along an aridity gradient. Glob Chang Biol 17:1108–1118

    Article  Google Scholar 

  • Tisdall JM, Oades J (1982) Organic matter and water-stable aggregates in soils. J Soil Sci 33:141–163

    Article  CAS  Google Scholar 

  • Turner NC, Molyneux N, Yang S, Xiong Y, Siddique KHM (2011) Climate change in south-west Australia and northwest China: challenges and opportunities for crop production. Crop Pasture Sci 62:445–456

    Article  Google Scholar 

  • Vanek SJ, Lehmann J (2014) Phosphorus availability to beans via interactions between mycorrhizas and biochar. Plant Soil 1–19

  • Verheijen F, Jeffery S, Bastos AC, van der Velde M, Diafas I (2010) Biochar application to soils—a critical scientific review of effects on soil properties, processes and functions. EUR 24099 EN. Office for the Official Publications of the European Communities, Luxembourg, p 149

    Google Scholar 

  • Warnock DD, Lehmann J, Kuyper TW, Rillig MC (2007) Mycorrhizal responses to biochar in soil—concepts and mechanisms. Plant Soil 300:9–20

    Article  CAS  Google Scholar 

  • Warnock DD, Mummey DL, McBride B, Major J, Lehmann J, Rillig MC (2010) Influences of non-herbaceous biochar on arbuscular mycorrhizal fungal abundances in roots and soils: results from growth-chamber and field experiments. Appl Soil Ecol 46:450–456

    Article  Google Scholar 

  • Wilson JM (1984) Comparative development of infection by three vesicular arbuscular mycorrhizal fungi. New Phytol 97:413–426

    Article  Google Scholar 

Download references

Acknowledgments

We appreciate the contributions of Ms Aimee Martin and Mr James Gee who volunteered their time in helping in the glasshouse, laboratory and potting rooms. Additionally, we thank the Soil Biology and Molecular Ecology Group at The University of Western Australia for providing the positive environment in which to conduct this experiment.

Author information

Authors and Affiliations

  1. Soil Biology and Molecular Ecology Group, School of Earth and Environment (M087), Crawley, Australia

    Bede S. Mickan, Lynette K. Abbott & Zakaria M. Solaiman

  2. UWA Institute of Agriculture, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Bede S. Mickan, Lynette K. Abbott, Katia Stefanova & Zakaria M. Solaiman

Authors
  1. Bede S. Mickan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lynette K. Abbott
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katia Stefanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zakaria M. Solaiman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bede S. Mickan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1

Dry shoot mass of Trifolium subterraneum in the bait chamber harvested at 35, 49, and 63 days after emergence (DAE) for the (a) water stressed (30 % field capacity) and (b) well watered treatments. BC = 2 % w/w biochar, NB = 0 % w/w biochar applied to the field chamber; WS = water stressed and WW = well watered treatments. Error bars show standard errors of the mean (n = 3). * significance p < 0.05. (PNG 27 kb)

Supplementary Fig. 2

Dry root mass of Trifolium subterraneum in the bait chamber harvested at 35, 49, and 63 days after emergence (DAE) for the (a) water stressed (30 % field capacity) and (b) well watered treatments. BC = 2 % w/w biochar, NB = 0 % w/w biochar applied to the field chamber; WS = water stressed and WW = well watered treatments. Error bars show standard errors of the mean (n = 3). * significance p < 0.05. (PNG 25 kb)

Supplementary Fig. 3

Hyphal length in soil in the bait chamber with distance (1, 5 and 9 cm) from the mesh barrier at 35 and 49 days after emergence (DAE) for well watered and water stressed treatments. WSBC = water stress/biochar, WWBC = well watered/biochar, WSNB = water stress/no biochar, WWNB = well watered/no biochar. Biochar applied to the field chamber only. Error bars show standard errors of the mean (n = 3). (PNG 36 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mickan, B.S., Abbott, L.K., Stefanova, K. et al. Interactions between biochar and mycorrhizal fungi in a water-stressed agricultural soil. Mycorrhiza 26, 565–574 (2016). https://doi.org/10.1007/s00572-016-0693-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-016-0693-4

Keywords

Search

Navigation